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Genome activity during the emergence of mouse embryonic totipotency (time course)

ABSTRACT: Fertilization transforms sperm and egg into a totipotent embryo but the underlying mechanisms are unknown. We here report that gene expression initiates during the gamete-to-embryo transition in mouse embryos. Meiotic exit induced by sperm entry enhances a transcriptionally-permissive epigenetic landscape. Time-course analysis of single embryos revealed a succession of genome-wide transcription 'ripples' initiating within 2 hours. Disrupting key pluripotency transcription factor levels prior to sperm entry had little immediate effect, indicating that different mechanisms engender pluripotent and totipotent states. These findings suggest that a hierarchical gene expression program characterizes the emergence of totipotency during the gamete-to-embryo transition, with broad mechanistic implications for the reprogramming of cellular potency.

ORGANISM(S): Mus musculus

PROVIDER: GSE64649 | GEO | 2023/03/02

SECONDARY ACCESSION(S): PRJNA271563

REPOSITORIES: GEO

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Genome activity during the emergence of mouse embryonic totipotency (morpholino)

Project description:Fertilization transforms sperm and egg into a totipotent embryo but the underlying mechanisms are unknown. We here report that gene expression initiates during the gamete-to-embryo transition in mouse embryos. Meiotic exit induced by sperm entry enhances a transcriptionally-permissive epigenetic landscape. Time-course analysis of single embryos revealed a succession of genome-wide transcription 'ripples' initiating within 2 hours. Disrupting key pluripotency transcription factor levels prior to sperm entry had little immediate effect, indicating that different mechanisms engender pluripotent and totipotent states. These findings suggest that a hierarchical gene expression program characterizes the emergence of totipotency during the gamete-to-embryo transition, with broad mechanistic implications for the reprogramming of cellular potency.

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Project description:The oocyte-to-embryo transition converts terminally differentiated gametes into a totipotent embryo. Fertilized embryos undergo the resetting of the transcriptional program as the zygotic genome is activated from a silenced state started from the late-stage oocyte. How transcriptome, translatome, and proteome interplay in this critical developmental window remains poorly understood. Utilizing a highly sensitive mass spectrometry, we obtained high-quality proteome landscapes including nearly 6,000 genes spanning 10 stages, from the mouse full-grown oocyte (FGO) to blastocyst, using 100 oocytes/embryos at each stage. By integrative analysis with corresponding transcriptomes and translatomes, we found transcription and translation levels can not reflect protein abundance in most cases. From FGOs to the 4-cell embryos, the proteomes are predominated by FGO-produced proteins, while the transcriptome and the translatome are much more dynamic. FGO-originated proteins frequently persist in embryos after the corresponding transcripts are already downregulated or decayed. Improved concordance between protein and RNA is observed for genes starting translation only upon meiotic resumption or transcribed only in embryos, although the detected protein dynamics often lag behind transcription and translation. Concordance between protein and transcription/translation is associated with protein half-lives. Finally, a kinetic model well predicts protein dynamics when incorporating both the initial protein abundance in FGO and translation kinetics across developmental stages. In sum, our study reveals multilayer control of gene expression during oocyte maturation and embryogenesis.

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